Abstract

Antioxidant systems modulate oxidant-based signaling networks and excessive removal of oxidants can prevent beneficial acclimation responses. Evidence from mutant, transgenic, and locally adapted natural plant systems is used to interpret differences in the capacity for antioxidation and formulate hypotheses for future inquiry. We focus on the first line of chloroplast antioxidant defense, pre-emptive thermal dissipation of excess absorbed light (monitored as nonphotochemical fluorescence quenching, NPQ) as well as on tocopherol-based antioxidation. Findings from NPQ-deficient and tocopherol-deficient mutants that exhibited enhanced biomass production and/or enhanced foliar water-transport capacity are reviewed and discussed in the context of the impact of lower levels of antioxidation on plant performance in hot/dry conditions, under cool temperature, and in the presence of biotic stress. The complexity of cellular redox-signaling networks is related to the complexity of environmental and endogenous inputs as well as to the need for intensified training and collaboration in the study of plant–environment interactions across biological sub-disciplines.

Introduction

The interplay between oxidant and antioxidant production is a hallmark of all living cells. While research in this area initially focused on beneficial effects of antioxidants, research in both biomedical (see, e.g., [13]) and botanical (see below) contexts has revised its focus due to the realization that excessive removal of oxidants can prevent beneficial acclimation responses.

While oxidation of macromolecules was initially universally viewed as damage, it is now clear that certain macromolecules are particularly sensitive to oxidation and serve as early-warning systems for rising internal oxidant production. For example, oxidation products of oxidation-prone polyunsaturated fatty acids serve as gene regulators that prompt increased antioxidant production and other responses [4,5]. Likewise, thiol-group-containing proteins are linked to redox-based gene-regulation [68]. Oxidation of these early-warning systems triggers enhanced antioxidant production as well as broad suites of additional adjustments in plant form and function. Antioxidant systems can thus be understood as modulators of oxidant-based signaling networks [9].

Plants increase antioxidant production when exposed to any of a variety of environmental stresses. The extensive body of work on this effect demonstrates antioxidant up-regulation in response to multiple stresses, which led to the assumption that engineering of crops for enhanced antioxidant production will be beneficial [1013]. However, key questions remain. How much antioxidant production is enough? How much is too much? Does the answer to this question depend on specific internal and external contexts? What trade-offs may be associated with differences in antioxidant production and setpoints of cellular redox state?

We review evidence for mutant, engineered, and natural, locally adapted plant systems that differ in their capacity to modulate the level of oxidants formed in photosynthesis through antioxidant processes directly associated with the light-processing system of leaves. The initial impetus for this review came from observations on a pair of Arabidopsis thaliana ecotypes locally adapted to different temperature and light regimes in Italy and Sweden [1416]. In particular, while the Swedish ecotype exhibited superior freezing tolerance [1719], the Italian ecotype exhibited faster rosette growth and more biomass accumulation as well as lesser capacities for two chloroplast-based antioxidation processes when grown under hot temperature or low light intensity [2025].

The following sections (i) briefly summarize the paradigm shift in how oxidants and antioxidants are viewed, (ii) provide an overview of the chloroplast-based antioxidant processes in which the Swedish and Italian ecotypes differed, and (iii) discuss different plant adaptation strategies and trade-offs associated with contrasting environments and plant growth habits as well as their implications for natural and agricultural systems.

Parallel progression in medical and plant science in understanding oxidants

Redox-signaling networks play particularly extensive roles in plants/autotrophs [9] that produce all of their antioxidants as needed, including tocopherols (vitamin E) and carotenoids that are the focus of this review. Furthermore, as sessile organisms, plants rely even more strongly on metabolic defenses than animals that often evade stressful environments through behavior. Stressful conditions can trigger genetic programs in plants that result in metabolic inactivation [26]. For instance, a complete inactivation of photosynthesis in overwintering evergreens—accompanied by a precipitous drop of photochemical energy-conversion efficiency to near-zero levels—results from responses that permit evergreen leaves and needles to be retained in environments with intense solar radiation and little or no opportunity to utilize this energy for metabolism [2731].

Earlier views on plant oxidative stress are undergoing re-examination, especially in light of the pressing need to develop climate-resilient, yet highly productive crops [32]. For example, Mittler provided a review entitled ‘ROS (reactive oxygen species) are good’ [33], where he stated: ‘ROS are predominantly beneficial to cells, supporting basic cellular processes and viability, and oxidative stress is only an outcome of a deliberate activation of a physiological cell death pathway’. Foyer et al. [34] added: ‘This is particularly true in photosynthesis, which is driven by large redox and energy gradients, and which is the major source of ROS in plant cells. ROS production, signaling and removal associated with photosynthesis provide flexibility and control in the management of high light stress. Grasping the implications of this paradigm shift is key to addressing global issues such as food security and the production of crops in a sustainable manner for a growing world population’.

These developments in plant science parallel similar paradigm shifts in other areas. In medical science, for example, an analogous trajectory led to the conclusion that: ‘Research efforts need to be redirected. [Oxidant-based change] is protective and is a misguided target for therapy’ [35].

Selected examples of chloroplast-based antioxidation: de-excitation, nonphotochemical quenching, and reduction by carotenoid and tocopherol

The chloroplast's role of harnessing solar energy makes it a key site of oxidant production. The following provides a brief overview of selected antioxidant metabolites (tocopherol, or vitamin E, and carotenoids) that interact with light harvesting; excellent recent reviews are available that provide more detail ([9,36]; see also chapters in Demmig-Adams et al. [37]). The energy of light absorbed by chlorophyll is channeled into the electron transport chain as long as the plant is able to utilize this energy and, for example, consumes photosynthetically produced sugars in growth, reproduction, or storage. If more light is absorbed than consumed, singlet-excited chlorophyll may be converted to triplet-excited chlorophyll that is capable of passing energy on to oxygen, resulting in ROS (singlet oxygen). Excess singlet-excited chlorophyll can be pre-emptively removed by the xanthophyll zeaxanthin (Zea) in cooperation with a pH-sensing protein, PsbS [3840]. The triplet-excited state of chlorophyll, once formed, can be de-excited by xanthophylls such as lutein [41]. Excitation energy that makes it all the way to oxygen can be removed via de-excitation of singlet oxygen by the antioxidant tocopherol (Toco; [42,43]).

When existing antioxidant levels are insufficient to remove excess excitation energy through the above-described mechanisms, oxidant-derived regulators up-regulate genes that serve in photoprotection and other acclimatory responses. Oxidation products of polyunsaturated lipids (oxylipins) are an example of such gene regulators. Regulation of the level of singlet-excited chlorophyll affects how many electrons flow into the photosynthetic electron transport chain and thereby modulates a host of additional redox-signaling relays. These redox networks involve reduced ROS, thiol-modulated metabolites and proteins, phosphorylation cascades, and, again, oxylipins [7,9,4446]. When excess-energy levels rise dramatically, oxidation of reaction-center proteins can shut down charge-separation as the source of high-energy electrons and incompletely reduced oxygen species [28,31,34,47]. Some authors have suggested that photoinhibition of photosynthesis is based on such an inactivation of primary photochemistry coupled with sustained engagement of photoprotective energy dissipation—as seen in overwintering evergreens (see above; [31,4750]) or in leaves grown under constant low light and suddenly exposed to dramatically higher light intensity [34,51].

Below, we focus mainly on the first line of chloroplast antioxidant defense—pre-emptive de-excitation of excited-state chlorophyll by conversion of excitation energy to harmless heat with the help of PsbS and Zea (Figure 1). This thermal dissipation process can be monitored from the associated decreases in chlorophyll fluorescence emission, or nonphotochemical quenching (NPQ; see [36] and chapters in Demmig-Adams et al. [37]). The level of NPQ is correlated with modulation of redox-signaling pathways that regulate gene expression (see above). Moreover, both Zea and Toco have dual antioxidant functions (Figure 1)—not only in thermal de-excitation of electronically excited reactive species but also in the full reduction of incompletely reduced ROS and/or lipid-peroxidation products [5254].

Schematic depiction of de-excitation and reduction processes in the chloroplast.

Figure 1.
Schematic depiction of de-excitation and reduction processes in the chloroplast.

De-excitation reactions include de-excitation of singlet-excited chlorophyll by zeaxanthin (Zea) in conjunction with PsbS as well as de-excitation of singlet oxygen by tocopherols (Toco). Reduction reactions include reduction in lipid peroxyl radicals by Zea and Toco as well as reduction in oxidized Toco or superoxide radical and its derivatives by antioxidant metabolites ascorbate and glutathione and associated enzyme systems. The shading in the figure from red to blue indicates the transition from antioxidation processes involving de-excitation of electronically excited states to reduction in reduced states. It should be noted that de-excitation of excited singlet chlorophyll by Zea and PsbS can involve either pure energy transfer or rapid, reversible exchange of an electron in a charge-transfer complex [39,40].

Figure 1.
Schematic depiction of de-excitation and reduction processes in the chloroplast.

De-excitation reactions include de-excitation of singlet-excited chlorophyll by zeaxanthin (Zea) in conjunction with PsbS as well as de-excitation of singlet oxygen by tocopherols (Toco). Reduction reactions include reduction in lipid peroxyl radicals by Zea and Toco as well as reduction in oxidized Toco or superoxide radical and its derivatives by antioxidant metabolites ascorbate and glutathione and associated enzyme systems. The shading in the figure from red to blue indicates the transition from antioxidation processes involving de-excitation of electronically excited states to reduction in reduced states. It should be noted that de-excitation of excited singlet chlorophyll by Zea and PsbS can involve either pure energy transfer or rapid, reversible exchange of an electron in a charge-transfer complex [39,40].

Trade-offs in the context of water use

After hearing a presentation on the proposed role of zeaxanthin in NPQ during the 1989 Rockefeller Foundation meeting on ‘The Potential of Biotechnology for Improving Grain Yield of Rice under Water Limited Conditions’ in Italy, Bill Ogren suggested that plants could be engineered with less Zea and NPQ to enhance productivity. This suggestion did not receive much interest until recently. Below, we review features of selected plant lines with impaired or naturally lower NPQ and tocopherol levels that exhibit features of interest, such as increased foliar water transport and/or increased plant growth under certain environmental conditions.

The need for climate-resilient crops is intensifying [32] as extreme weather becomes more common, including greater heat/drought in the summer. In his review entitled ‘Safety conscious or living dangerously’, Murchie [36] posed the question, ‘what is the ‘right’ level of plant photoprotection for fitness and productivity?’ This may vary dependent on the combination of specific environmental conditions and genotype. In the context of water use, annual (herbaceous, fast-growing, short-lived) plants must replenish the high levels of water lost from their leaves under hot dry conditions to sustain the high productivity needed for expedient completion of their life cycle within a single year. A greater capacity to distribute water throughout leaves is presumably coupled with other adaptations, including a larger root volume for improved underground water mining (see, e.g., [55]. However, this strategy would not be successful when water availability in the soil decreases below a minimal level. For example, during recent decades of selection for higher yields, the overall sensitivity of corn to drought and high evaporative demand has also increased [56]. The latter authors emphasized that the challenges of low precipitation and high evaporative demand need to be considered individually.

A review on abiotic stress tolerance entitled ‘To grow or not to grow: a stressful decision for plants’ [57] addresses contrasting responses to drought—including accelerated growth, slowed growth, or complete growth arrest. For example, in arid and desert environments, a plethora of different strategies are employed by a variety of species, all of which are successful in their own way [5860]. Soft-leafed annuals or desert ephemerals specialize in accelerated growth and complete their life cycle before drought sets in. In contrast, many other species arrest their growth and persist through periods of reduced water availability as evergreens or perennials that drop leaves or stems, or even persist solely as underground storage organs until sufficient precipitation returns. The approach of accelerated growth by desert annuals during a transient favorable period with high water availability may be a relevant model for irrigated annual crops with access to enough water to support continued carbon dioxide uptake under hot/dry conditions by continually replacing water lost in transpiration.

For the example of the C3 species A. thaliana, adaptations of the leaf's water-transport system have also been demonstrated. An A. thaliana accession (Col-0) originating from a site that is relatively dry for A. thaliana but not in absolute terms (558 mm annual average precipitation in the Landsberg an der Warthe region in Poland; see [15]) exhibited more pronounced up-regulation of transpiration rate (Figure 2A), of the density of minor leaf veins (Figure 2B), and of the proportion of each minor vein comprised of water conduits (Figure 2C) compared with an accession (Castelnuovo-12, sub-line 24) from a moister site (818 mm average annual precipitation in Castelnuovo di Porto, Italy; [14,15]) in response to growth at hot versus cool temperature under controlled conditions [15]. In other words, an adaptation of A. thaliana to relatively low precipitation led to a greater capacity of the leaf's water-moving vascular infrastructure under hot growth temperature with high evaporative demand [57]. This annual mesophyte's response is quite different from that of species found in much drier sites, such as woody species that restrict both water transport and growth under drought, while lessening leaf heat load via angled and/or highly reflective leaves (see discussion in [15]).

Phenotypic plasticity in transpiration rate and foliar water transport infrastructure in Arabidopsis thaliana accessions adapted to different levels of precipitation.

Figure 2.
Phenotypic plasticity in transpiration rate and foliar water transport infrastructure in Arabidopsis thaliana accessions adapted to different levels of precipitation.

(A) Transpiration rate (mmol H2O m–2 s–1), (B) minor vein density (mm minor vein length mm–2 leaf area), and (C) the ratio of water to sugar conduits (ratio of tracheary to sieve elements) in minor veins for leaves of two accessions of A. thaliana originating from sites with mean annual precipitation of 818 mm (Italy [14]) and 558 mm (Poland) when grown under a day/night leaf temperature of 14°C/12.5°C (blue columns) or 36°C/25°C (blue plus purple columns) under a 9-h photoperiod of 400 µmol photons m–2 s–1. The vapor-pressure difference between leaf and air was 0.85 and 2.01 kPa under cool and hot growth temperature, respectively. Data from Adams et al. [15]. Growing plants at both high temperature (top of purple columns) as well as cool temperature (top of blue columns) allowed assessment of the degree of up-regulation in hot-grown plants (blue plus purple portion of columns) relative to cool-grown plants (blue portion of columns).

Figure 2.
Phenotypic plasticity in transpiration rate and foliar water transport infrastructure in Arabidopsis thaliana accessions adapted to different levels of precipitation.

(A) Transpiration rate (mmol H2O m–2 s–1), (B) minor vein density (mm minor vein length mm–2 leaf area), and (C) the ratio of water to sugar conduits (ratio of tracheary to sieve elements) in minor veins for leaves of two accessions of A. thaliana originating from sites with mean annual precipitation of 818 mm (Italy [14]) and 558 mm (Poland) when grown under a day/night leaf temperature of 14°C/12.5°C (blue columns) or 36°C/25°C (blue plus purple columns) under a 9-h photoperiod of 400 µmol photons m–2 s–1. The vapor-pressure difference between leaf and air was 0.85 and 2.01 kPa under cool and hot growth temperature, respectively. Data from Adams et al. [15]. Growing plants at both high temperature (top of purple columns) as well as cool temperature (top of blue columns) allowed assessment of the degree of up-regulation in hot-grown plants (blue plus purple portion of columns) relative to cool-grown plants (blue portion of columns).

As mentioned in the Introduction section, another set of studies reported that the A. thaliana accession adapted to the relatively mild/warm climate in Italy had a lower capacity for NPQ [21,23,25] as well as lower tocopherol levels [21,22] under certain growth conditions (including hot temperature) than an accession (Rodasen-47, sub-line 29) from Sweden (Rödåsen, Sweden; [14]) with its much colder climate [15]. Future studies would be of interest that assess whether additional accessions adapted to contrasting local temperature and precipitation regimes also differ in the capacity of these antioxidants as well as, possibly, additional antioxidant systems.

Moreover, several studies on NPQ-deficient and/or tocopherol-deficient mutants of A. thaliana and other species addressed the hypothesis that these mutants exhibit leaf features that enable faster replacement of water lost in transpiration. Several A. thaliana mutants deficient in these foliar antioxidant systems (Figure 3) indeed exhibited such features when grown under hot temperature, i.e., a greater density of foliar veins and more water conduits per vein [23,61,62] that are thought to enhance the ability of leaves to replace water lost under high evaporative demand [15,63]. Consistent with these results from A. thaliana, an NPQ-deficient tobacco line with reduced PsbS and NPQ levels exhibited greater stomatal conductance, and tobacco lines with enhanced NPQ (via PsbS overexpression) exhibited lesser stomatal conductance when grown under field conditions [64].

Effect of antioxidant deficiency on foliar vein composition in Arabidopsis thaliana.

Figure 3.
Effect of antioxidant deficiency on foliar vein composition in Arabidopsis thaliana.

Ratio of water conduits (tracheary elements) to sugar conduits (sieve elements) in minor foliar veins of A. thaliana wild-type (WT Col-0; open columns), the tocopherol-deficient mutant vte1 (black columns), and the NPQ-impaired mutant npq1 npq4 (gray column) grown in (A) a naturally lit glasshouse or (B) under hot temperature in a climate-controlled growth chamber. Water-to-sugar conduit ratio was expressed on a basis of conduit cross-sectional area per vein, and in each case normalized by multiplying the ratios × vein density that was also significantly greater in both mutants compared with WT. Arabidopsis thaliana data from Stewart et al. [23,62]; significant differences between WT and mutants are indicated with asterisks (** P < 0.01; *** P < 0.001).

Figure 3.
Effect of antioxidant deficiency on foliar vein composition in Arabidopsis thaliana.

Ratio of water conduits (tracheary elements) to sugar conduits (sieve elements) in minor foliar veins of A. thaliana wild-type (WT Col-0; open columns), the tocopherol-deficient mutant vte1 (black columns), and the NPQ-impaired mutant npq1 npq4 (gray column) grown in (A) a naturally lit glasshouse or (B) under hot temperature in a climate-controlled growth chamber. Water-to-sugar conduit ratio was expressed on a basis of conduit cross-sectional area per vein, and in each case normalized by multiplying the ratios × vein density that was also significantly greater in both mutants compared with WT. Arabidopsis thaliana data from Stewart et al. [23,62]; significant differences between WT and mutants are indicated with asterisks (** P < 0.01; *** P < 0.001).

It may be rewarding to test whether tuning antioxidant levels to match varying water availability over the course of the growing season in regions without access to irrigation may allow plants to shift between (i) fast growth and low water-use efficiency when precipitation is available and (ii) reduced growth and high water-use efficiency during intermittent drought periods (see, e.g., [65]).

The A. thaliana accession from Italy that exhibited lower intrinsic NPQ capacity as well as lower tocopherol levels than the Swedish accession when grown at hot temperatures under high evaporative demand (see above) showed similarly diminished antioxidant features when grown under low light intensity [20,25]. Likewise, mutant systems with altered NPQ dynamics suggest a link between light-use efficiency and NPQ in the context of plant productivity. Tobacco engineered for accelerated disengagement of energy dissipation (accelerated NPQ relaxation) upon transition from excessively high to low light levels limiting to photosynthesis exhibited greater carbon uptake in low light as well as accumulation of significantly more biomass [66,67]. When excitation energy is no longer excessive and no other stresses are present, disengagement of energy dissipation occurs via a drop in ΔpH and removal of zeaxanthin. The tobacco leaves were engineered for either accelerated ΔpH abolishment [66] or accelerated removal of zeaxanthin [67].

It may be rewarding to address the hypothesis that this increased biomass accumulation in plant lines with lower chloroplast-based antioxidation results not only from additional available excitation energy and carbon gain in limiting light but also from possible formation of greater ROS levels and growth stimulation by oxidative signals. Future studies should quantify ROS levels in systems that return to high photochemical efficiency at different speeds subsequent to high-light exposure. Signaling processes can have profound effects on plant growth irrespective of light supply [68,69]. Future research should thus address the relative contributions to increased photosynthetic productivity from two different mechanisms: (i) reduced loss of photons via lowered thermal dissipation (i.e., reduced waste of photons) versus (ii) altered cellular redox-signaling with the outcome of maintaining, for example, stomatal opening for continued productivity under hot/arid conditions. The evidence reviewed here (e.g., that both NPQ-deficient mutants and tocopherol-deficient mutants exhibit increased support for foliar water transport when grown at hot temperature) points to the importance of redox modulation. While NPQ-impaired mutants concomitantly lower thermal dissipation of absorbed photons and also impact cellular redox state, the tocopherol-deficient mutant featured here exhibited unaltered thermal-dissipation capacity (see Stewart et al. [23] for NPQ capacity in hot-grown vte1), and presumably acts exclusively through its impact on cellular redox state. The similar effect of these two mutant systems on foliar water transport (Figure 3) suggests redox modulation as the common mechanism for this effect.

Growth rates did differ between the A. thaliana accession from Sweden with the higher NPQ capacity and higher tocopherol levels and the Italian accession with the lower NPQ capacity and lower tocopherol levels in low-light- or hot-grown leaves. The Swedish accession produced much smaller rosettes and less biomass than the Italian accession under either low growth light intensity or hot growth temperature [2022,70]. While this finding supports a hypothesis that lesser NPQ/tocopherol levels may be associated with growth stimulation by oxidative signals under certain environmental conditions, it is important to keep in mind that these two natural accessions differ in multiple regulatory networks (e.g., [19]), of which redox-regulatory systems are just one component.

Trade-offs in the context of temperature

The evidence discussed above suggests that rapid replacement of lost water under hot conditions in annual C3 species via greater foliar vein density and more water conduits per vein may be associated with a shift of the cellular redox state to more oxidizing conditions. The question arises whether the converse would be true for cool conditions, i.e., that a shift of the cellular redox state to more reducing conditions may be beneficial. Identification of possible trade-offs in plant performance in hot–dry versus cool-moist environments is important since the current increase in extreme weather events includes not only greater heat and/or drought, but also late-spring/early-fall cold spells (Intergovernmental Panel on Climate Change; http://www.ipcc.ch).

While greater intrinsic NPQ capacity and tocopherol levels in the Swedish versus the Italian accessions of A. thaliana were reported specifically for plants grown under low light intensity and/or hot temperature (see above), no such data are available for plants grown under high light and/or cold temperature. Future characterization should thus be extended to additional environmental growth conditions. In the meantime, there is indirect evidence supporting the hypothesis that the Swedish accession may, in fact, produce greater rather than lesser concentrations of oxidant-derived oxylipin gene regulators in either cold- or high-light-grown leaves than the Italian accession. This indirect evidence stems from three lines of inquiry detailed below on cell wall ingrowths in foliar sugar-loading cells as affected by genotype and experimental oxylipin treatment.

Cool temperature diminishes plant productivity by lowering the activity of proteins, including enzymes involved in carbon fixation [71] and transporters involved in sugar export from leaves. Expedient sugar export from leaves is important to maintaining high levels of photosynthesis because sugar build-up in leaves can activate feedback that leads to repression of photosynthetic proteins (see [72]). The Swedish accession exhibited greater up-regulation of intrinsic photosynthetic capacity (Figure 4A) as well as of the number (Figure 4B) and cell wall invaginations of phloem cells involved in loading sugar into export conduits (Figure 4C) in cool- versus warm-grown leaves than the Italian accession [73]. Both greater numbers and wall ingrowths [22,73] of these phloem cells enhance the membrane area available for placement of transport proteins that support sucrose loading (see discussion in [16,24]).

Phenotypic plasticity in photosynthetic capacity and foliar sugar-transport infrastructure in Arabidopsis thaliana accessions adapted to different temperatures.

Figure 4.
Phenotypic plasticity in photosynthetic capacity and foliar sugar-transport infrastructure in Arabidopsis thaliana accessions adapted to different temperatures.

Up-regulation of (A) maximal intrinsic photosynthetic capacity [light- and CO2-saturated oxygen evolution (µmol O2 m–2 s–1) determined at 25°C], (B) number of phloem loading cells per minor vein, and (C) phloem (parenchyma) cell wall ingrowths (percent increase) in leaves of two ecotypes of A. thaliana [14] originating from sites with mean annual temperatures of 15°C (Italy) and 3°C (Sweden) when grown at a day/night leaf temperature of 14°C/12.5°C (red plus purple columns) compared with 36°C/25°C (red columns) under a 9-h photoperiod of 400 µmol photons m–2 s–1. Data from Adams et al. [15]. Growing plants at both high temperature (top of red columns) as well as cool temperature (top of purple columns) allowed assessment of the degree of up-regulation in cool-grown relative to hot-grown plants (purple portion of columns).

Figure 4.
Phenotypic plasticity in photosynthetic capacity and foliar sugar-transport infrastructure in Arabidopsis thaliana accessions adapted to different temperatures.

Up-regulation of (A) maximal intrinsic photosynthetic capacity [light- and CO2-saturated oxygen evolution (µmol O2 m–2 s–1) determined at 25°C], (B) number of phloem loading cells per minor vein, and (C) phloem (parenchyma) cell wall ingrowths (percent increase) in leaves of two ecotypes of A. thaliana [14] originating from sites with mean annual temperatures of 15°C (Italy) and 3°C (Sweden) when grown at a day/night leaf temperature of 14°C/12.5°C (red plus purple columns) compared with 36°C/25°C (red columns) under a 9-h photoperiod of 400 µmol photons m–2 s–1. Data from Adams et al. [15]. Growing plants at both high temperature (top of red columns) as well as cool temperature (top of purple columns) allowed assessment of the degree of up-regulation in cool-grown relative to hot-grown plants (purple portion of columns).

It was, furthermore, shown that treatment with jasmonate (methyl jasmonate, MeJA) enhanced wall invagination of phloem cells in A. thaliana (Figure 5) [74]. A similar enhancement was seen in an NPQ-impaired A. thaliana mutant compared with its wild-type (WT) (Figure 5) [53]. These results support the hypothesis that less photoprotection, and resulting enhanced oxylipin production [53,75,76], could be beneficial under cool growth temperature in annual species. Future studies into the antioxidant capacity of cool-grown leaves should address a broader variety of antioxidant processes and their possible differential adjustment in response to environmental conditions.

Effect of the phytohormone methyl jasmonate or antioxidant deficiency on foliar sugar-loading cell ultrastructure and effect of antioxidant deficiency on lipid-peroxidation-based messengers.

Figure 5.
Effect of the phytohormone methyl jasmonate or antioxidant deficiency on foliar sugar-loading cell ultrastructure and effect of antioxidant deficiency on lipid-peroxidation-based messengers.

Phloem parenchyma cell wall ingrowths in leaves of A. thaliana wild-type (WT; open columns) compared with WT treated with methyl jasmonate (MeJA; hatched column) and the NPQ-impaired npq1 lut2 mutant (black column) as well as the level of foliar oxylipins in WT compared with the NPQ-impaired mutants npq1 (dark-gray column) and npq4 (medium-gray column) and the tocopherol-deficient mutant vte1 (light-gray column). The double mutant npq1 lut2 is missing the enzyme that forms Zea from its violaxanthin precursor and is also missing lutein (that is implicated in de-excitation of the secondary excited state of chlorophyll, triplet-chlorophyll; [41]). In A. thaliana, cell wall invaginations are formed in phloem parenchyma cells that facilitate sugar loading by flooding the apoplastic space surrounding the companion cells and sieve elements with both sucrose (via sucrose efflux channels) and protons (via ATPases). Data from [53,7476].

Figure 5.
Effect of the phytohormone methyl jasmonate or antioxidant deficiency on foliar sugar-loading cell ultrastructure and effect of antioxidant deficiency on lipid-peroxidation-based messengers.

Phloem parenchyma cell wall ingrowths in leaves of A. thaliana wild-type (WT; open columns) compared with WT treated with methyl jasmonate (MeJA; hatched column) and the NPQ-impaired npq1 lut2 mutant (black column) as well as the level of foliar oxylipins in WT compared with the NPQ-impaired mutants npq1 (dark-gray column) and npq4 (medium-gray column) and the tocopherol-deficient mutant vte1 (light-gray column). The double mutant npq1 lut2 is missing the enzyme that forms Zea from its violaxanthin precursor and is also missing lutein (that is implicated in de-excitation of the secondary excited state of chlorophyll, triplet-chlorophyll; [41]). In A. thaliana, cell wall invaginations are formed in phloem parenchyma cells that facilitate sugar loading by flooding the apoplastic space surrounding the companion cells and sieve elements with both sucrose (via sucrose efflux channels) and protons (via ATPases). Data from [53,7476].

Vascular tissue is an attractive target of jasmonic acid (JA) signaling since JA is not only synthesized in the plastids of phloem cells but is also transported over long-distances through the phloem [7779]. Future studies should address whether JA may also be involved in the adjustment of water conduit number and vein density shown in Figure 3. Overall, oxylipin gene regulators should be a rewarding target of future investigation into the impact of chloroplast antioxidant capacity on plant growth, development, and stress response, since enzymatic lipid peroxidation by lipoxygenase (LOX) is activated via oxidation of LOX's catalytic iron center by ROS and inactivated via reduction of this iron by tocopherols [80]. Other hormones, like auxins that are known to orchestrate vascular differentiation [81], may also be involved since biosynthesis, degradation, and signaling of multiple plant hormones is under redox control [82,83].

In addition to evaluating both sugar- and water-transport components of the foliar vasculature, future studies should consider specific features of individual water conduits that protect against tension-induced conduit collapse under high evaporative demand (thicker cell walls; see, e.g., [84,85]) or against freeze–thaw-induced embolism (narrower conduits; see, e.g., [8688]). Both tocopherol-deficient and NPQ-deficient A. thaliana mutants exhibited an intriguing combination [23,61,62] of greater vein density and greater water-conduit numbers (as features with putative benefits under heat/drought) with narrower water conduits (as a feature with putative benefits under freeze–thaw cycles).

Beyond abiotic conditions: biotic defense, NPQ, and tocopherol

In the context of effects of redox state on foliar vascular organization illustrated by Figures 2 and 3, it should be noted that many pathogenic viruses, bacteria, and fungi spread through the plant vasculature [8991]. Modulation of foliar vascular organization, among other defense-related responses, should thus receive further attention as a target of signaling cross-talk and cross-tolerance of abiotic and biotic stress. A PsbS-deficient mutant of rice exhibited greater resistance against fungal and bacterial pathogens [92]. Similarly, the PsbS-deficient npq4 mutant of A. thaliana exhibited superior defense against herbivory by caterpillars [93] and spider mites [94] compared with WT. It should be noted, however, that seed production was reduced in the PsbS-deficient npq4 mutant of A. thaliana under field conditions [95]. To identify possible trade-offs, a comprehensive characterization of biotic and abiotic stress responses is needed under multiple environmental conditions and in multiple genotypes.

In addition to their role in biotic defense, chloroplast-based redox-signaling networks can themselves be the target of invaders [96]. For example, the necrotrophic pathogen Sclerotinia sclerotiorum causes a decrease in intra-thylakoid pH associated with stimulation of Zea and NPQ formation as well as a drop in violaxanthin that is not only a precursor of Zea but also of the plant hormone abscisic acid (ABA) with its roles in stomatal closure and defense responses [97]. Increased stomatal opening facilitates pathogen entry into the leaf and compromised defense further facilitates infection [97]. This pathogen thus manipulates Zea and thermal dissipation levels to enhance its ability to infect plants. These results further highlight the need for comprehensive studies into the impact of antioxidant-capacity modulation under multiple environmental challenges.

Redox-signaling networks mirror complexity over space and time in environmental and endogenous contexts

The remarkable complexity of redox-signaling networks mirrors that of whole-plant response to a wide range of specific environments with myriad combinations of abiotic and biotic influences [60,98]. Environmental cues are perceived and integrated by transduction systems involving the interaction of ROS, antioxidants, phytohormones, and sugars with transcription factors that modulate stress tolerance, programmed cell death, growth, and development [45,99]. ROS can either promote or suppress growth by having different effects on cell cycle and programmed cell death and depending on the specific type of ROS and tissue involved, plant developmental state and source–sink balance, and the kind of environmental stress encountered [33,100].

Rather than representing a single optimal setpoint that provides homeostasis of metabolism, oxidant/antioxidant-balance setpoints may differ dependent on the external environment and genetic differences in adaptation to local environmental conditions. Shifts in these setpoints may have occurred over the course of plant evolution and also take place during plant development.

Esteban et al. [101] proposed an evolutionary shift from greater emphasis on pre-emptive de-excitation of excess singlet-excited chlorophyll via Zea-associated NPQ to a greater emphasis on detoxification of ROS once formed by tocopherol, which could be seen as shifting from being more ‘safety conscious’ to ‘living dangerously’ (see above; [36]) as terrestrial environments and climate became more variable. A follow-up hypothesis could be formulated stating that the relative emphasis also differs between fast-growing herbaceous and slow-growing woody species with their very different intrinsic NPQ capacities (i.e., determined under experimental conditions that allow only enough electron transport to maintain trans-thylakoid pH) [31].

Moreover, shifts in photoprotection also occur during the progression through plant life stages. For example, Juvany et al. [102] reported that females of a Mediterranean tree species lowered both NPQ and tocopherol levels and increased LOX activity, all of which presumably increased oxylipin production, when entering their reproductive phase. Such a down-regulation of antioxidant capacity may serve to enhance the production of oxidant-based orchestrators of reproduction.

Conclusions and outlook

The existing evidence indicates that both environmental and endogenous conditions shift the setpoint for the balance between oxidation and antioxidation. Further work is needed that places photoprotection via chloroplast-based antioxidant processes in the context of redox-signaling networks controlling plant growth, development, and stress response [103]. Such investigation should be conducted in whole plants [104] under a variety of environmental conditions and with multiple genotypes. Specific environmental conditions should include both abiotic and biotic factors and their variation over the course of days and seasons in the context of different plant genetic and developmental features (see [69]). These comprehensive approaches will require intensification of discipline-transcending training and collaboration across molecular science, genetics/genomics, functional biology, ecology, and evolutionary biology.

Abbreviations

     
  • ABA

    abscisic acid

  •  
  • JA

    jasmonic acid

  •  
  • LOX

    lipoxygenase

  •  
  • MeJA

    methyl jasmonate

  •  
  • NPQ

    nonphotochemical quenching of chlorophyll fluorescence

  •  
  • PsbS

    photosystem II subunit S

  •  
  • ROS

    reactive oxygen species

  •  
  • Toco

    tocopherols

  •  
  • WT

    wild type

  •  
  • Zea

    Zeaxanthin

Acknowledgements

We thankfully acknowledge support from the National Science Foundation [award DEB-1022236] and the University of Colorado at Boulder.

Competing Interests

The Authors declare that there are no competing interests associated with the manuscript.

References

References
1
Gomez-Cabrera
,
M.-C.
,
Domenech
,
E.
,
Romagnoli
,
M.
,
Arduini
,
A.
,
Borras
,
C.
,
Pallardo
,
F.V.
et al (
2008
)
Oral administration of vitamin C decreases muscle mitochondrial biogenesis and hampers training-induced adaptations in endurance performance
.
Am. J. Clin. Nutr.
87
,
142
149
2
Jackson
,
M.J.
(
2008
)
Free radicals generated by contracting muscle: by-products of metabolism or key regulators of muscle function?
Free Radic. Biol. Med.
44
,
132
141
3
Adams
,
R.B.
,
Egbo
,
K.N.
and
Demmig-Adams
,
B.
(
2014
)
High-dose vitamin C supplements diminish the benefits of exercise in athletic training and disease prevention
.
Nutr. Food Sci.
44
,
95
101
4
Mosblech
,
A.
,
Feussner
,
I.
and
Heilmann
,
I.
(
2009
)
Oxylipins: structurally diverse metabolites from fatty acid oxidation
.
Plant Physiol. Biochem.
47
,
511
517
5
Kuhn
,
H.
,
Banthiya
,
S.
and
van Leyen
,
K.
(
2015
)
Mammalian lipoxygenases and their biological relevance
.
Biochim. Biophys. Acta, Mol. Cell Biol.
1851
,
308
330
6
Lee
,
S.
,
Kim
,
S.M.
and
Lee
,
R.T.
(
2013
)
Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance
.
Antioxid. Redox Signal.
18
,
1165
1207
7
Dietz
,
K.-J.
and
Hell
,
R.
(
2015
)
Thiol switches in redox regulation of chloroplast: balancing redox state, metabolism and oxidative stress
.
Biol. Chem.
396
,
483
494
8
Martins
,
L.
,
Trujillo-Hernandez
,
J.A.
and
Reichheld
,
J.-P.
(
2018
)
Thiol based redox signaling in plant nucleus
.
Front. Plant Sci.
9
,
705
9
Noctor
,
G.
,
Reichheld
,
J.-P.
and
Foyer
,
C.H.
(
2018
)
ROS-related redox regulation and signaling in plants
.
Semin. Cell Dev. Biol.
80
,
3
12
10
Ahmad
,
P.
,
Jaleel
,
C.A.
,
Salem
,
M.A.
,
Nabi
,
G.
and
Sharma
,
S.
(
2010
)
Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress
.
Crit. Rev. Biotechnol.
30
,
161
175
11
Gill
,
S.S.
and
Tuteja
,
N.
(
2010
)
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants
.
Plant Physiol. Biochem.
48
,
909
930
12
Tang
,
X.
,
Mu
,
X.
,
Shao
,
H.
,
Wang
,
H.
and
Brestic
,
M.
(
2015
)
Global plant-responding mechanisms to salt stress: physiological and molecular levels and implications in biotechnology
.
Crit. Rev. Biotechnol.
35
,
425
437
13
You
,
J.
and
Chan
,
Z.
(
2015
)
ROS regulation during abiotic stress responses in crop plants
.
Front. Plant Sci.
6
,
1092
14
Ågren
,
J.
and
Schemske
,
D.W.
(
2012
)
Reciprocal transplants demonstrate strong adaptive differentiation of the model organism Arabidopsis thaliana in its native range
.
New Phytol.
194
,
1112
1122
15
Adams
, III,
W.W.
,
Stewart
,
J.J.
,
Cohu
,
C.M.
,
Muller
,
O.
and
Demmig-Adams
,
B.
(
2016
)
Habitat temperature and precipitation of Arabidopsis thaliana ecotypes determine the response of foliar vasculature, photosynthesis, and transpiration to growth temperature
.
Front. Plant Sci.
7
,
1026
16
Adams
, III,
W.W.
,
Stewart
,
J.J.
,
Polutchko
,
S.K.
and
Demmig-Adams
,
B.
(
2018
) Leaf vasculature and the upper limit of photosynthesis. In
The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration
(
Adams
,
W.W.,
III
and
Terashima
,
I.
, eds), vol.
44
, pp.
27
54
,
Springer
,
The Netherlands
17
Oakley
,
C.G.
,
Ågren
,
J.
,
Atchison
,
R.A.
and
Schemske
,
D.W.
(
2014
)
QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs
.
Mol. Ecol.
23
,
4304
4315
18
Gehan
,
M.A.
,
Park
,
S.
,
Gilmour
,
S.J.
,
An
,
C.
,
Lee
,
C.-M.
and
Thomashow
,
M.F.
(
2015
)
Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes
.
Plant J.
84
,
682
693
19
Park
,
S.
,
Gilmour
,
S.J.
,
Grumet
,
R.
and
Thomashow
,
M.F.
(
2018
)
CBF-dependent and CBF-independent regulatory pathways contribute to the differences in freezing tolerance and cold-regulated gene expression of two Arabidopsis ecotypes locally adapted to sites in Sweden and Italy
.
PLoS ONE
13
,
e0207723
20
Cohu
,
C.M.
,
Lombardi
,
E.
,
Adams
, III,
W.W.
and
Demmig-Adams
,
B.
(
2014
)
Increased nutritional quality of plants for long-duration spaceflight missions through choice of plant variety and manipulation of growth conditions
.
Acta Astronaut.
94
,
799
806
21
Stewart
,
J.J.
,
Adams
, III,
W.W.
,
Cohu
,
C.M.
,
Polutchko
,
S.K.
,
Lombardi
,
E.M.
and
Demmig-Adams
,
B.
(
2015
)
Differences in light-harvesting, acclimation to growth light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana
.
Planta
242
,
1277
1290
22
Stewart
,
J.J.
,
Demmig-Adams
,
B.
,
Cohu
,
C.M.
,
Wenzl
,
C.A.
,
Muller
,
O.
and
Adams
, III,
W.W.
(
2016
)
Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and Southern Europe
.
Plant Cell Environ.
39
,
1549
1558
23
Stewart
,
J.J.
,
Baker
,
C.R.
,
Sharpes
,
C.S.
,
Wong-Michalak
,
S.T.
,
Polutchko
,
S.K.
,
Adams
, III,
W.W.
et al (
2018
)
Effects of foliar redox status on leaf vascular organization suggest avenues for cooptimization of photosynthesis and heat tolerance
.
Int. J. Mol. Sci.
19
,
2507
24
Demmig-Adams
,
B.
,
Stewart
,
J.J.
,
Baker
,
C.R.
and
Adams
, III,
W.W.
(
2018
)
Optimization of photosynthetic productivity in contrasting environments by regulons controlling plant form and function
.
Int. J. Mol. Sci.
19
,
872
25
Oakley
,
C.G.
,
Savage
,
L.
,
Lotz
,
S.
,
Larson
,
G.R.
,
Thomashow
,
M.F.
,
Kramer
,
D.M.
et al (
2018
)
Genetic basis of photosynthetic responses to cold in two locally adapted populations of Arabidopsis thaliana
.
J. Exp. Bot.
69
,
699
709
26
Wagner
,
D.
,
Przybyla
,
D.
,
Op den Camp
,
R.
,
Kim
,
C.
,
Landgraf
,
F.
,
Lee
,
K.P.W.
et al (
2004
)
The genetic basis of singlet oxygen-induced stress responses of Arabidopsis thaliana
.
Science
306
,
1183
1185
27
Adams
, III,
W.W.
,
Demmig-Adams
,
B.
,
Verhoeven
,
A.S.
and
Barker
,
D.H.
(
1995
)
‘Photoinhibition’ during winter stress: involvement of sustained xanthophyll cycle-dependent energy dissipation
.
Aust. J. Plant Physiol.
22
,
261
276
28
Adams
, III,
W.W.
,
Zarter
,
C.R.
,
Mueh
,
K.E.
,
Amiard
,
V.
and
Demmig-Adams
,
B.
(
2008
) Energy dissipation and photoinhibition: a continuum of photoprotection. In
Photoprotection, Photoinhibition, Gene Regulation, and Environment. Advances in Photosynthesis and Respiration
(
Demmig-Adams
,
B.
,
Adams
,
W.W.,
III
, and
Mattoo
,
A.K.
, eds), vol.
40
, pp.
49
64
,
Springer
,
The Netherlands
29
Zarter
,
C.R.
,
Adams
, III,
W.W.
,
Ebbert
,
V.
,
Cuthbertson
,
D.
,
Adamska
,
I.
and
Demmig-Adams
,
B.
(
2006
)
Winter downregulation of intrinsic photosynthetic capacity coupled with upregulation of Elip-like proteins and persistent energy dissipation in a subalpine forest
.
New Phytol.
172
,
272
282
30
Zarter
,
C.R.
,
Adams
, III,
W.W.
,
Ebbert
,
V.
,
Adamska
,
I.
,
Jansson
,
S.
and
Demmig-Adams
,
B.
(
2006
)
Winter acclimation of PsbS and related proteins in the evergreen Arctostaphylos uva-ursi as influenced by altitude and light environment
.
Plant Cell Environ.
29
,
869
878
31
Demmig-Adams
,
B.
and
Adams
, III,
W.W.
(
2006
)
Photoprotection in an ecological context: the remarkable complexity of thermal dissipation
.
New Phytol.
172
,
11
21
32
Dhanker
,
O.M.
and
Foyer
,
C.H.
(
2018
)
Climate resilient crops for improving global food security and safety
.
Plant Cell Environ.
41
,
877
884
33
Mittler
,
R.
(
2017
)
ROS are good
.
Trends Plant Sci.
22
,
11
19
34
Foyer
,
C.H.
,
Ruban
,
A.V.
and
Noctor
,
G.
(
2017
)
Viewing oxidative stress through the lens of oxidative signalling rather than damage
.
Biochem. J.
474
,
877
883
35
Naviaux
,
R.K.
(
2012
)
Oxidative shielding or oxidative stress?
J. Pharmacol. Exp. Ther.
342
,
608
618
36
Murchie
,
E.H.
(
2017
)
Safety conscious or living dangerously: what is the ‘right’ level of plant photoprotection for fitness and productivity?
Plant Cell Environ.
40
,
1239
1242
37
Demmig-Adams
,
B.
,
Garab
,
G.
,
Adams
,
W.W.
and
Govindjee
(eds.), (
2014
)
Non-photochemical quenching and thermal energy dissipation in plants, algae and cyanobacteria.
Springer
,
Dordrecht, The Netherlands
.
38
Li
,
X.-P.
,
Björkman
,
O.
,
Shih
,
C.
,
Grossman
,
A.R.
,
Rosenquist
,
M.
,
Jansson
,
S.
et al (
2001
)
A pigment-binding protein essential for regulation of photosynthetic light harvesting
.
Nature
403
,
391
395
39
Park
,
S.
,
Fischer
,
A.L.
,
Steen
,
C.J.
,
Iwai
,
M.
,
Morris
,
J.M.
,
Walla
,
P.J.
et al (
2018
)
Chlorophyll-carotenoid excitation energy transfer in high-light-exposed thylakoid membranes investigated by snapshot transient absorption spectroscopy
.
J. Am. Chem. Soc.
140
,
11965
11973
40
Park
,
S.
,
Steen
,
C.
,
Lyska
,
D.
,
Fischer
,
A.L.
,
Endelman
,
B.
,
Iwai
,
M.
et al (
2019
)
Chlorophyll-carotenoid excitation energy transfer and charge transfer in Nannochloropsis oceanica for the regulation of photosynthesis
.
Proc. Natl Acad. Sci. U.S.A.
116
,
3385
3390
41
Dall'Osto
,
L.
,
Lico
,
C.
,
Alric
,
J.
,
Giuliano
,
G.
,
Havaux
,
M.
and
Bassi
,
R.
(
2006
)
Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light
.
BMC Plant Biol.
6
,
32
42
Rastogi
,
A.
,
Yadav
,
D.K.
,
Szymańska
,
R.
,
Kruk
,
J.
,
Sedlářová
,
M.
and
Pospíšil
,
P.
(
2014
)
Singlet oxygen scavenging activity of tocopherol and plastochromanol in Arabidopsis thaliana: relevance to photooxidative stress
.
Plant Cell Environ.
37
,
392
401
43
Havaux
,
M.
,
Eymery
,
F.
,
Porfirova
,
S.
,
Rey
,
P.
and
Dörmann
,
P.
(
2005
)
Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana
.
Plant Cell
17
,
3451
3469
44
Baginsky
,
S.
and
Gruissem
,
W.
(
2009
)
The chloroplast kinase network: new insights from large-scale phosphoproteome profiling
.
Mol. Plant
2
,
1141
1153
45
Foyer
,
C.H.
and
Noctor
,
H.
(
2009
)
Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications
.
Antioxid. Redox Signal.
11
,
861
905
46
Munné-Bosch
,
S.
,
Queval
,
G.
and
Foyer
,
C.H.
(
2013
)
The impact of global change factors on redox signaling underpinning stress tolerance
.
Plant Physiol.
161
,
5
19
47
Adams
, III,
W.W.
,
Zarter
,
C.R.
,
Ebbert
,
V.
and
Demmig-Adams
,
B.
(
2004
)
Photoprotective strategies of overwintering evergreens
.
BioScience
54
,
41
49
48
Savitch
,
L.V.
,
Leonardos
,
E.D.
,
Krol
,
M.
,
Jansson
,
S.
,
Grodzinski
,
B.
,
Huner
,
N.P.A.
et al (
2002
)
Two different strategies for light utilization in photosynthesis in relation to growth and cold acclimation
.
Plant Cell Environ.
25
,
761
771
49
Öquist
,
G.
and
Hüner
,
N.P.A.
(
2003
)
Photosynthesis of overwintering evergreen plants
.
Annu. Rev. Plant Biol.
54
,
329
355
50
Verhoeven
,
A.
(
2014
)
Sustained energy dissipation in winter evergreens
.
New Phytol.
201
,
57
65
51
Demmig-Adams
,
B.
,
Moeller
,
D.L.
,
Logan
,
B.A.
and
Adams
, III,
W.W.
(
1998
)
Positive correlation between levels of retained zeaxanthin plus antheraxanthin and degree of photoinhibition in shade leaves of Schefflera arboricola (Hayata) Merrill
.
Planta
205
,
367
374
52
Munné-Bosch
,
S.
(
2005
)
The role of α-tocopherol in plant stress tolerance
.
J. Plant Physiol.
162
,
743
748
53
Demmig-Adams
,
B.
,
Cohu
,
C.M.
,
Amiard
,
V.
,
van Zadelhoff
,
G.
,
Veldink
,
G.A.
,
Muller
,
O.
et al (
2013
)
Emerging trade-offs — impact of photoprotectants (PsbS, xanthophylls, and vitamin E) on oxylipins as regulators of development and defense
.
New Phytol.
197
,
720
729
54
Havaux
,
M.
and
García-Plazaola
,
J.I.
(
2014
) Beyond non-photochemical fluorescence quenching: the overlapping antioxidant functions of zeaxanthin and tocopherols. In
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration
(
Demmig-Adams
,
B.
,
Garab
,
G.
,
Adams
, III,
W.W.
and
Govindjee
, eds.), vol.
40
, pp.
583
603
,
Springer
,
The Netherlands
55
Killi
,
D.
,
Bussotti
,
F.
,
Raschi
,
A.
and
Haworth
,
M.
(
2017
)
Adaptation to high temperature mitigates the impact of water deficit during combined heat and drought stress in C3 sunflower and C4 maize varieties with contrasting drought tolerance
.
Physiol. Plant.
159
,
130
147
56
Lobell
,
D.B.
,
Roberts
,
M.J.
,
Schlenker
,
W.
,
Braun
,
N.
,
Little
,
B.B.
,
Rejesus
,
R.M.
et al (
2014
)
Greater sensitivity to drought accompanies maize yield increase in the US Midwest
.
Science
344
,
516
519
57
Dolferus
,
R.
(
2014
)
To grow or not to grow: a stressful decision for plants
.
Plant Sci.
229
,
247
261
58
Demmig-Adams
,
B.
,
Dumlao
,
M.R.
,
Herzenach
,
M.K.
and
Adams
, III,
W.W.
(
2008
)
Acclimation
. In
Behavioral Ecology
(
Jørgensen
,
S.E.
and
Fath
,
B.D.
, eds.), pp.
15
23
,
Elsevier
,
Oxford
59
Adams
, III,
W.W.
and
Demmig-Adams
,
B.
(
2014
) Lessons from nature: a personal perspective. In
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration
(
Demmig-Adams
,
B.
,
Garab
,
G.
,
Adams
, III,
W.W.
and
Govindjee
, eds.), vol.
40
, pp.
45
72
,
Springer
,
The Netherlands
60
Adams
, III,
W.W.
,
Stewart
,
J.J.
and
Demmig-Adams
,
B.
(
2018
) Photosynthetic modulation in response to plant activity and the environment. In
The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration
(
Adams
, III,
W.W.
and
Terashima
,
I.
, eds.), vol.
44
, pp.
493
563
,
Springer
,
The Netherlands
61
Stewart
,
J.J.
,
Polutchko
,
S.K.
,
Adams
, III,
W.W.
,
Cohu
,
C.M.
,
Wenzl
,
C.A.
and
Demmig-Adams
,
B.
(
2017
)
Light, temperature, and tocopherol status influence foliar vascular anatomy and leaf function in Arabidopsis thaliana
.
Physiol. Plant.
160
,
98
110
62
Stewart
,
J.J.
,
Adams
, III,
W.W.
,
Cohu
,
C.M.
and
Demmig-Adams
,
B.
(
2018
)
Tocopherols modulate leaf vein arrangement and composition without impacting photosynthesis
.
Photosynthetica
56
,
382
391
63
Dunbar-Co
,
S.
,
Sporck
,
M.J.
and
Sack
,
L.
(
2009
)
Leaf trait diversification and design in seven rare taxa of the Hawaiian Plantago radiation
.
Int. J. Plant Sci.
170
,
61
75
64
Glowacka
,
K.
,
Kromdijk
,
J.
,
Kucera
,
K.
,
Xie
,
J.
,
Cavanagh
,
A.P.
,
Leonelli
,
L.
et al (
2018
)
Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop
.
Nat. Commun.
9
,
868
65
Yadav
,
O.P.
(
2010
)
Drought response of pearl millet landrace-based populations and their crosses with elite composites
.
Field Crop. Res.
118
,
51
56
66
Armbruster
,
U.
,
Leonelli
,
L.
,
Correa Galvis
,
V.
,
Strand
,
D.
,
Quinn
,
E.H.
,
Jonikas
,
M.C.
et al (
2016
)
Regulation and levels of the thylakoid K+/H+ antiporter KEA3 shape the dynamic response of photosynthesis in fluctuating light
.
Plant Cell Physiol.
57
,
1557
1567
67
Krondijk
,
J.
,
Glowacka
,
K.
,
Leonelli
,
L.
,
Gabilly
,
S.T.
,
Iwai
,
M.
,
Niyogi
,
K.K.
et al (
2016
)
Improving photosynthesis by accelerating recovery from photoprotection
.
Science
354
,
857
861
68
Downs
,
R.J.
(
1962
) Photocontrol of growth and dormancy in woody plants. In
Tree Growth
(
Kozlowski
,
T.T.
, ed.), pp.
133
149
,
Ronald Press
,
U.S.A.
69
Demmig-Adams
,
B.
,
Stewart
,
J.J.
and
Adams
, III,
W.W.
(
2017
)
Environmental regulation of intrinsic photosynthetic capacity: an integrated view
.
Curr. Opin. Plant Biol.
37
,
34
41
70
Stewart
,
J.J.
,
Polutchko
,
S.K.
,
Adams
, III,
W.W.
and
Demmig-Adams
,
B.
(
2017
)
Acclimation of Swedish and Italian ecotypes of Arabidopsis thaliana to light intensity
.
Photosynth. Res.
134
,
215
229
71
Berry
,
J.
and
Björkman
,
O.
(
1980
)
Photosynthetic response and adaptation to temperature in higher plants
.
Ann. Rev. Plant Physiol.
31
,
491
543
72
Krapp
,
A.
and
Stitt
,
M.
(
1995
)
An evaluation of direct and indirect mechanisms for the ‘sink-regulation’ of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves
.
Planta
195
,
313
323
73
Adams
, III,
W.W.
,
Cohu
,
C.M.
,
Amiard
,
V.
and
Demmig-Adams
,
B.
(
2014
)
Associations between the acclimation of phloem-cell wall ingrowths in minor veins and maximal photosynthesis rate
.
Front. Plant Sci.
5
,
24
74
Amiard
,
V.
,
Demmig-Adams
,
B.
,
Mueh
,
K.E.
,
Turgeon
,
R.
,
Combs
,
A.F.
and
Adams
, III,
W.W.
(
2007
)
Role of light and jasmonic acid signaling in regulating foliar phloem cell wall ingrowth development
.
New Phytol.
173
,
722
731
75
Munné-Bosch
,
S.
,
Weiler
,
E.W.
,
Alegre
,
L.
,
Müller
,
M.
,
Püchting
,
P.
and
Falk
,
J.
(
2007
)
α-Tocopherol may influence cellular signaling by modulating jasmonic acid levels in plants
.
Planta
225
,
681
691
76
Frenkel
,
M.
,
Külheim
,
C.
,
Jänkänpää
,
H.J.
,
Skogström
,
O.
,
Dall'Osto
,
L.
,
Ågren
,
J.
et al (
2009
)
Improper excess light energy dissipation in Arabidopsis results in a metabolic reprogramming
.
BMC Plant Biol.
9
,
12
77
Hause
,
B.
,
Hause
,
G.
,
Kutter
,
C.
,
Miersch
,
O.
and
Wasternack
,
C.
(
2003
)
Enzymes of jasmonate biosynthesis occur in tomato sieve elements
.
Plant Cell Physiol.
44
,
643
648
78
Stenzel
,
I.
,
Hause
,
B.
,
Maucher
,
H.
,
Pitzschke
,
A.
,
Mierch
,
O.
,
Ziegler
,
J.
et al (
2003
)
Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato — amplification in wound signalling
.
Plant J.
33
,
577
589
79
Howe
,
G.A.
and
Schilmiller
,
A.L.
(
2002
)
Oxylipin metabolism in response to stress
.
Curr. Opin. Plant Biol.
5
,
230
236
80
Maccarrone
,
M.
,
Manca-di-Villahermosa
,
S.
,
Meloni
,
C.
,
Massoud
,
R.
,
Mascali
,
A.
,
Guarina
,
R.
et al (
1999
)
Arachidonate cascade, apoptosis, and Vitamin E in peripheral blood mononuclear cells from hemodialysis patients
.
Am. J. Kidney Dis.
40
,
600
610
81
Furuta
,
K.M.
,
Hellmann
,
E.
and
Helariutta
,
Y.
(
2014
)
Molecular control of cell specification and cell differentiation during procambial development
.
Annu. Rev. Plant Biol.
65
,
607
638
82
Srivastava
,
A.K.
,
Redij
,
T.
,
Sharma
,
B.
and
Suprasanna
,
P.
(
2017
) Interaction between hormone and redox signaling in plants: divergent pathways and convergent roles. In
Mechanism of Plant Hormone Signaling Under Stress, II
(
Pandey
,
G.K.
, ed.), pp.
1
22
,
John Wiley & Sons, Inc
,
U.S.A.
83
Tognetti
,
V.B.
,
Bielach
,
A.
and
Hrtyan
,
M.
(
2017
)
Redox regulation at the site of primary growth: auxin, cytokinin and ROS crosstalk
.
Plant Cell Environ.
40
,
2586
2605
84
Blackman
,
C.J.
,
Gleason
,
S.M.
,
Cook
,
A.M.
,
Chang
,
Y.
,
Laws
,
C.A.
and
Westoby
,
M.
(
2018
)
The links between leaf hydraulic vulnerability to drought and key aspects of leaf venation and xylem anatomy among 26 Australian woody angiosperms from contrasting climates
.
Ann. Bot.
122
,
59
67
85
Cardoso
,
A.A.
,
Brodribb
,
T.J.
,
Lucani
,
C.J.
,
DaMatta
,
F.M.
and
McAdam
,
S.A.M.
(
2018
)
Coordinated plasticity maintains hydraulic safety in sunflower leaves
.
Plant Cell Environ.
11
,
2567
2576
86
Tyree
,
M.T.
,
Davis
,
S.D.
and
Cochard
,
H.
(
1994
)
Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction
.
IAWA J.
15
,
335
360
87
Pittermann
,
J.
and
Sperry
,
J.
(
2003
)
Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers
.
Tree Physiol.
23
,
907
914
88
Gleason
,
S.M.
,
Blackman
,
C.J.
,
Gleason
,
S.T.
,
McCulloh
,
K.A.
,
Ocheltree
,
T.W.
and
Westoby
,
M.
(
2018
)
Vessel scaling in evergreen angiosperm leaves conforms with Murray's law and area-filling assumptions: implications for plant size, leaf size and cold tolerance
.
New Phytol.
218
,
1360
1370
89
Vuorinen
,
A.L.
,
Kelloniemi
,
J.
and
Valkonen
,
J.P.T.
(
2011
)
Why do viruses need phloem for systemic invasion of plants?
Plant Sci.
181
,
355
363
90
Hipper
,
C.
,
Brault
,
V.
,
Ziegler-Graff
,
V.
and
Revers
,
F.
(
2013
)
Viral and cellular factors involved in phloem transport of plant viruses
.
Front. Plant Sci.
4
,
154
91
Yadeta
,
K.A.
and
Thomma
,
P.H.J.
(
2013
)
The xylem as battleground for plant hosts and vascular wilt pathogens
.
Front. Plant Sci.
4
,
97
92
Zulfugarov
,
I.S.
,
Tovuu
,
A.
,
Kim
,
C.-Y.
,
Vo
,
K.T.X.
,
Ko
,
S.Y.
,
Hall
,
M.
et al (
2016
)
Enhanced resistance of PsbS-deficient rice (Oryza sativa L.) to fungal and bacterial pathogens
.
J. Plant Biol.
59
,
616
626
93
Jänkänpää
,
J.H.
,
Frenkel
,
M.
,
Zulfugarov
,
I.S.
,
Reichelt
,
M.
,
Krieger- Liszkay
,
A.
,
Mishra
,
Y.
et al (
2013
)
Non-photochemical quenching capacity in Arabidopsis thaliana affects herbivore behaviour
.
PLoS One
8
,
e53232
94
Barczak-Brzyzek
,
A.K.
,
Kiełkiewicz
,
M.
,
Gawronski
,
P.
,
Kot
,
K.
,
Filipecki
,
M.
and
Karpinska
,
B.
(
2017
)
Cross-talk between high light stress and plant defence to the two-spotted spider mite in Arabidopsis thaliana
.
Exp. Appl. Acarol.
73
,
177
189
95
Külheim
,
C.
,
Ågren
,
L.
and
Jansson
,
S.
(
2002
)
Rapid regulation of light harvesting and plant fitness in the field
.
Science
5578
,
91
93
96
Trotta
,
A.
,
Rahikainen
,
M.
,
Konert
,
G.
,
Finazzi
,
G.
and
Kangasjärvi
,
S.
(
2014
)
Signalling crosstalk in light stress and immune reactions in plants
.
Philos. Trans. R. Soc. B
369
,
20130235
97
Zhou
,
J.
,
Zeng
,
L.
,
Liu
,
J.
and
Xing
,
D.
(
2015
)
Manipulation of the xanthophyll cycle increases plant susceptibility to Sclerotinia sclerotiorum
.
PLoS Pathog.
11
,
e1004878
98
Demmig-Adams
,
B.
,
Stewart
,
J.J.
and
Adams
, III,
W.W.
(
2014
)
Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment
.
Philos. Trans. R. Soc. B
369
,
20130244
99
Schippers
,
J.H.M.
,
Foyer
,
C.H.
and
van Dongen
,
J.T.
(
2016
)
Redox regulation in shoot growth, SAM maintenance and flowering
.
Curr. Opin. Plant Biol.
29
,
121
128
100
Schmidt
,
R.
,
Kunkowska
,
A.B.
and
Schippers
,
J.H.M.
(
2016
)
Role of reactive oxygen species during cell expansion in leaves
.
Plant Physiol.
172
,
2098
2106
101
Esteban
,
R.
,
Olano
,
J.M.
,
Castresana
,
J.
,
Fernández-Marín
,
B.
,
Hernández
,
A.
,
Becerril
,
J.M.
et al (
2009
)
Distribution and evolutionary trends of photoprotective isoprenoids (xanthophylls and tocopherols) within the plant kingdom
.
Physiol. Plant.
135
,
379
389
102
Juvany
,
M.
,
Mueller
,
M.
,
Pinto-Marijuan
,
M.
and
Munne-Bosch
,
S.
(
2014
)
Sex-related differences in lipid peroxidation and photoprotection in Pistacia lentiscus
.
J. Exp. Bot.
65
,
1039
1049
103
Demmig-Adams
,
B.
,
Stewart
,
J.J.
,
Burch
,
T.A.
and
Adams
, III,
W.W.
(
2014
)
Insights from placing photosynthetic light harvesting into context
.
J. Phys. Chem. Lett.
5
,
24
104
Adams
, III,
W.W.
,
Muller
,
O.
,
Cohu
,
C.M.
and
Demmig-Adams
,
B.
(
2014
) Photosystem II efficiency and non-photochemical quenching in the context of source-sink balance. In
Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria. Advances in Photosynthesis and Respiration
(
Demmig-Adams
,
B.
,
Garab
,
G.
,
Adams
, III,
W.W.
and
Govindjee
, eds), vol.
40
, pp.
503
529
,
Springer
,
The Netherlands